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The Risk of Colorectal Cancer in Patients with Ulcerative Colitis

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The Risk of Colorectal Cancer in Patients with Ulcerative Colitis Dig Dis Sci (2015) 60:492–501 DOI 10.1007/s10620-014-3373-2 ORIGINAL ARTICLE The Risk of Colorectal Cancer in Patients with Ulcerative Colitis Tobias M. Nowacki • Markus Bru¨ckner • Maria Eveslage • Phil Tepasse • Friederike Pott • Nils H. Thoennissen • Karin Hengst • Matthias Ross • Dominik Bettenworth Received: 11 April 2014 / Accepted: 24 September 2014 / Published online: 4 October 2014 Ó Springer Science+Business Media New York 2014 Abstract associated with the risk of CAC (P \ 0.0014); disease Background and Aim Ulcerative colitis increases the risk duration between 9 and 15 years: OR of 2.5 (95 % CI of developing dysplasia and colitis-associated cancer 0.2–41.1), more than 15 years: OR of 21.4 (95 % CI (CAC). The purpose of this study was to determine the risk 2.6–173.6). The risk of developing dysplasia (low-grade factors as well as protective measures for disease burden, intraepithelial neoplasia, LGIEN and high-grade intraepi- need for colectomy and the development of CAC in thelial neoplasia, HGIEN) or the need to undergo colec- ulcerative colitis (UC) patients. tomy was also significantly related to disease duration Methods A cohort of n = 434 UC patients was evaluated. (P = 0.006, P = 0.002, respectively). Established anti- Data analysis was performed by univariate and multivariate inflammatory medication (e.g., 5-ASA, anti-TNF-a) sig- logistic regression. Odds ratios (OR) and 95 % confidence nificantly reduced the risk of both dysplasia and CAC intervals (CI) were calculated, and significance was (P = 0.02). assessed by the likelihood ratio test. Conclusions Despite the use of modern therapies for UC, Results Mean patient age at UC diagnosis was CAC rates remain high. In our study, risk factors included 45.7 ± 15.1 years which manifested mainly as pancolitis disease duration while anti-inflammatory therapies reduced (47 %) or left-sided colitis (45.2 %). CAC was detected in the risk. Effective control of the intestinal inflammation ten patients (2.3 %). UC disease duration was strongly also reduced the disease burden as indicated by decreased risk of requiring colectomy, underscoring the need for sufficient surveillance and anti-inflammatory therapies. Tobias M. Nowacki, Markus Bru¨ckner, Matthias Ross and Dominik Bettenworth have contributed equally to this work. T. M. Nowacki Á M. Bru¨ckner Á P. Tepasse Á F. Pott Á M. Eveslage K. Hengst Á D. Bettenworth (&) Institute of Biostatistics and Clinical Research, University Department of Medicine B, University Hospital Mu¨nster, Mu¨nster, Mu¨nster, Germany Albert-Schweitzer-Campus 1, 48149 Mu¨nster, Germany e-mail: [email protected] e-mail: [email protected] N. H. Thoennissen T. M. Nowacki Department of Hematology and Oncology, Hubertus Wald e-mail: [email protected] Tumorzentrum, University Cancer Center Hamburg, University M. Bru¨ckner Medical Center Hamburg-Eppendorf, Hamburg, Germany e-mail: [email protected] e-mail: [email protected] P. Tepasse M. Ross e-mail: [email protected] Christophorus-Kliniken GmbH, St.-Vincenz-Hospital Coesfeld, F. Pott Coesfeld, Germany e-mail: [email protected] e-mail: [email protected] K. Hengst e-mail: [email protected] 123 Dig Dis Sci (2015) 60:492–501 493 Keywords Inflammatory bowel disease (IBD) Á delayed or missed in 18–27 % of UC patients [19, 20], a Ulcerative colitis (UC) Á Colitis-associated cancer (CAC) Á problem compounded by low patient uptake of surveillance Colorectal cancer Á Surveillance programs offered to those with long-standing extensive colitis [21]. Repetitive colonic inflammation not only fuels the Introduction disease burden for the individual patient but also increases the risk to require colectomy and colectomy- Chronic colonic inflammation is a well-known risk factor free survival rates have been proposed as a measurement for the development of colorectal malignancy [1]. Patients of therapeutic effectiveness [22]. Yet, risk factors for the with ulcerative colitis (UC) are at particularly increased need for colectomy are not well established. risk of developing colitis-associated cancer (CAC) [2, 3]. The aim of the present study was to evaluate risk factors While the incidence of sporadic colorectal cancer (CRC) for colectomy, development of dysplasia (LGIEN, HGIEN) is increased from the fifth decade of life, and maximal in and colon cancer, as well as to determine protective mea- the eighth decade, the median age of CAC diagnosis is sures in a relatively large cohort of UC patients at a tertiary 43 years [4, 5]. CAC has a significant impact on UC referral center. patients, with cause-specific mortality due to CRC sig- nificantly higher in UC patients compared to the back- ground population. Munkholm et al. [6] demonstrated Methods 15 % of all deaths in UC patients to be a consequence of CRC. Validated risk factors for CAC are helpful to Enrollment of Patients and Data Collection stratify the individual patients’ risk and include severity and duration of disease, primary sclerosing cholangitis We retrospectively analyzed 434 patients treated as (PSC) as well as a positive family history for CRC [7– inpatients or outpatients between 2002 and 2013 at the 11]. Department of Gastroenterology, University Hospital of Historically, the risk of CAC was first reported in a Mu¨nster, a tertiary referral center for IBD patients in pediatric cohort. Devrode et al. [12] found the risk to be northwestern Germany. Patients with UC as principle 20 % per decade beginning 10 years after diagnosis. More diagnosis were identified by searching for code K51 recently, a large meta-analysis including 116 studies (International Classification of Diseases, version 10, revealed incidence rates corresponding to cumulative ICD-10). Additionally, patients with both UC and colo- probabilities of 2 % by 10 years, 8 % by 20 years and rectal cancer were identified by search for codes C18; 18 % by 30 years of disease duration [8]. In the same C19; and C20. Diagnosis of UC was based on clinical study, the overall prevalence of CRC was reported to be presentation, exclusion of infectious enteritis and colitis 3.7 % (95 % CI 3.2–4.2 %). In contrast, a recent study as well as endoscopic and histopathological findings. from Denmark found no increased incidence of CAC and Data on demographics (age and sex), disease character- was confirmed by another study including 32,991 UC istics including duration (time elapsed since initial patients that found no increase in CAC over a 30-year diagnosis), disease severity (assessed by Mayo score) and period [13, 14]. In accordance with these findings, a more manifestations (location and extent of disease (deter- recent meta-analysis by Jess et al. [15] only found CAC mined as the maximal extent of colonic involvement: occurring in 1.6 % of UC patients within 14 years of proctitis, left-sided colitis or pancolitis according to the diagnosis which is significantly less compared to the Montreal classification [23])) were collected from studies described earlier [8]. patient’s clinical records (shown in Tables 1, 2)ina Endoscopic surveillance programs for detection of pre- cross-sectional analysis. Additionally, data on colitis- cancerous dysplasia have been evaluated for IBD patients related proctocolectomy, presence and grade of any and been proven to facilitate a reduced colorectal carci- dysplasia and CAC, as well as colitis-related specific noma-related mortality rate [16, 17]. Current guidelines anti-inflammatory and immunosuppressive medication recommend to begin screening colonoscopy, including were collected. random biopsies every 10 cm of bowel, in UC patients with Of 455 patients, 21 patients (5.2 %) were excluded from more than one-third of the colon involved 8–10 years after our analysis due to insufficient data being available; leav- initial diagnosis [18]. Subsequently, colonoscopy is sug- ing a total 434 patients included. Of these patients, any gested every 1–2 years in UC patients, and annually in with missing or unavailable data within a single category patients diagnosed with PSC. However, even when led to exclusion of that patient from that specific analysis screening complies with guidelines, CAC diagnosis is only, rather than from the study. 123 494 Dig Dis Sci (2015) 60:492–501 Table 1 Demographic and clinical data of patients with UC as Table 2 Demographic and clinical data of patients with CAC principle diagnosis (n = 434) (n = 10) Mean age ± SD 45.7 ± 15.1 Mean age ± SD 54.7 ± 17.3 Males/females 255 (58.8)/179 Males/females 5/5 (41.2) Max. extent of disease Max. extent of disease Proctitis 0 Proctitis 27 (7.8) Proctosigmoiditis/colitis of left colon 4 Proctosigmoiditis/colitis of left colon 156 (45.2) Pancolitis 6 Pancolitis 162 (47) Duration of disease Duration of disease Initial diagnosis 0 Initial diagnosis 23 (6) 1–8 years 1 1–8 years 189 (49.3) 9–15 years 1 9–15 years 84 (21.9) [15 years 8 [15 years 87 (22.7) Mayo score Mayo score 0–3 4 0–3 136 (44.2) 4–6 1 4–6 51 (16.6) 7–9 – 7–9 61 (19.8) 10–12 2 10–12 60 (19.5) Unknown 3 Presentation of dysplasia Presentation of dysplasia No dysplasia detected 322 (92.3) No dysplasia detected 0 Low-grade intraepithelial neoplasia 12 (3.4) Low-grade intraepithelial neoplasia (LGIEN) 0 (LGIEN) High-grade intraepithelial neoplasia (HGIEN) 0 High-grade intraepithelial neoplasia 5 (1.4) Invasive colon carcinoma 10 (HGIEN) Proctocolectomy Invasive colon carcinoma 10 (2.3) Yes 10 Colitis-associated colectomy No 0 Yes 74 (17.4) Extraintestinal manifestation No 352 (82.6) No extraintestinal manifestation 6 Extraintestinal manifestation Arthropathy 1 No extraintestinal manifestation 322 (80.5) Erythema nodosum 0 Arthropathy 40 (10) Primary sclerosing cholangitis 3 Erythema nodosum 5 (1.3) Uveitis 0 Primary sclerosing cholangitis 31 (7.8) Death Uveitis 2 (0.5) Yes 2 Values are given as total numbers with valid percentages in paren- No 8 theses unless stated otherwise Values are given as total numbers unless stated otherwise Assessment of Disease Activity and Histological Analysis from the visit at detection of any dysplasia, respectively.
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